Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots
Sucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB) and III, with dicot-specific Type I and monocot-s...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2014-11-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fpls.2014.00615/full |
| _version_ | 1811302052499816448 |
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| author | Duo ePeng Xi eGu Liangjiao eXue Liangjiao eXue Liangjiao eXue James H Leebens-Mack James H Leebens-Mack Chung-Jui eTsai Chung-Jui eTsai Chung-Jui eTsai |
| author_facet | Duo ePeng Xi eGu Liangjiao eXue Liangjiao eXue Liangjiao eXue James H Leebens-Mack James H Leebens-Mack Chung-Jui eTsai Chung-Jui eTsai Chung-Jui eTsai |
| author_sort | Duo ePeng |
| collection | DOAJ |
| description | Sucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB) and III, with dicot-specific Type I and monocot-specific Type IIB functioning in phloem loading. To shed light on the underlying drivers of SUT evolution, Bayesian phylogenetic inference was undertaken using 41 sequenced plant genomes, including seven basal lineages at key evolutionary junctures. Our analysis supports four phylogenetically and structurally distinct SUT subfamilies, originating from two ancient groups (AG1 and AG2) that diverged early during terrestrial colonization. In both AG1 and AG2, multiple intron acquisition events in the progenitor vascular plant established the gene structures of modern SUTs. Tonoplastic Type III and plasmalemmal Type II represent evolutionarily conserved descendants of AG1 and AG2, respectively. Type I and Type IIB were previously thought to evolve after the dicot-monocot split. We show, however, that divergence of Type I from Type III SUT predated basal angiosperms, likely associated with evolution of vascular cambium and phloem transport. Type I SUT was subsequently lost in monocots along with vascular cambium, and independent evolution of Type IIB coincided with modified monocot vasculature. Both Type I and Type IIB underwent lineage-specific expansion. In multiple unrelated taxa, the newly-derived SUTs exhibit biased expression in reproductive tissues, suggesting a functional link between phloem loading and reproductive fitness. Convergent evolution of Type I and Type IIB for SUT function in phloem loading and reproductive organs supports the idea that differential vascular development in dicots and monocots is a strong driver for SUT family evolution in angiosperms. |
| first_indexed | 2024-04-13T07:21:02Z |
| format | Article |
| id | doaj.art-2d4fe1681edc451188d82d61eadec77c |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-13T07:21:02Z |
| publishDate | 2014-11-01 |
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| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-2d4fe1681edc451188d82d61eadec77c2022-12-22T02:56:37ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2014-11-01510.3389/fpls.2014.00615119718Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicotsDuo ePeng0Xi eGu1Liangjiao eXue2Liangjiao eXue3Liangjiao eXue4James H Leebens-Mack5James H Leebens-Mack6Chung-Jui eTsai7Chung-Jui eTsai8Chung-Jui eTsai9University of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaUniversity of GeorgiaSucrose transporters (SUTs) are essential for the export and efficient movement of sucrose from source leaves to sink organs in plants. The angiosperm SUT family was previously classified into three or four distinct groups, Types I, II (subgroup IIB) and III, with dicot-specific Type I and monocot-specific Type IIB functioning in phloem loading. To shed light on the underlying drivers of SUT evolution, Bayesian phylogenetic inference was undertaken using 41 sequenced plant genomes, including seven basal lineages at key evolutionary junctures. Our analysis supports four phylogenetically and structurally distinct SUT subfamilies, originating from two ancient groups (AG1 and AG2) that diverged early during terrestrial colonization. In both AG1 and AG2, multiple intron acquisition events in the progenitor vascular plant established the gene structures of modern SUTs. Tonoplastic Type III and plasmalemmal Type II represent evolutionarily conserved descendants of AG1 and AG2, respectively. Type I and Type IIB were previously thought to evolve after the dicot-monocot split. We show, however, that divergence of Type I from Type III SUT predated basal angiosperms, likely associated with evolution of vascular cambium and phloem transport. Type I SUT was subsequently lost in monocots along with vascular cambium, and independent evolution of Type IIB coincided with modified monocot vasculature. Both Type I and Type IIB underwent lineage-specific expansion. In multiple unrelated taxa, the newly-derived SUTs exhibit biased expression in reproductive tissues, suggesting a functional link between phloem loading and reproductive fitness. Convergent evolution of Type I and Type IIB for SUT function in phloem loading and reproductive organs supports the idea that differential vascular development in dicots and monocots is a strong driver for SUT family evolution in angiosperms.http://journal.frontiersin.org/Journal/10.3389/fpls.2014.00615/fullAngiospermsPhloemtransportersmolecular evolutionexpression partitioningvascular evolution |
| spellingShingle | Duo ePeng Xi eGu Liangjiao eXue Liangjiao eXue Liangjiao eXue James H Leebens-Mack James H Leebens-Mack Chung-Jui eTsai Chung-Jui eTsai Chung-Jui eTsai Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots Frontiers in Plant Science Angiosperms Phloem transporters molecular evolution expression partitioning vascular evolution |
| title | Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots |
| title_full | Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots |
| title_fullStr | Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots |
| title_full_unstemmed | Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots |
| title_short | Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots |
| title_sort | bayesian phylogeny of sucrose transporters ancient origins differential expansion and convergent evolution in monocots and dicots |
| topic | Angiosperms Phloem transporters molecular evolution expression partitioning vascular evolution |
| url | http://journal.frontiersin.org/Journal/10.3389/fpls.2014.00615/full |
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